Disruption of activity in the ventral premotor but not the anterior intraparietal area interferes with on-line correction to a haptic perturbation during grasping

Abstract

Replanning ongoing movements following perturbations requires the accurate and immediate estimation of the motor response based on sensory input. Previous studies have used transcranial magnetic stimulation (TMS) in humans to demonstrate the participation of the anterior intraparietal sulcus (aIPS) and ventral premotor cortex (PMv) in visually mediated state estimation for grasping. Here, we test the role of parietofrontal circuits in processing the corrective responses to haptic perturbations of the finger during prehension. Subjects reached to grasp an object while having to compensate for a novel and unpredictable haptic perturbation of finger extension. TMS-based transient disruptions to the PMv and aIPS were delivered 0, 50, or 100 ms after the perturbation. TMS to the PMv delivered 50 ms after the perturbation (but not 0 or 100 ms, or in unperturbed trials) led to an overestimation of grasp aperture. No effects on grasp aperture were noted for the aIPS. Our results indicate that the PMv (but not aIPS) is involved in the deployment of the compensatory response in the presence of haptic perturbations during prehension. Our data also identify the time window of neural processing in the PMv when reprogramming occurs to be 50-100 ms following the perturbation onset.

Keywords: TMS; frontoparietal; grasping; haptic perturbation; on-line control; updating.

Conflict of interest statement

The authors declare no competing financial interests.

Copyright © 2015 the authors 0270-6474/15/352112-06$15.00/0.

Figures

Figure 1.

a, b, Finger–wrist trajectories for No PERT and PERT trials in a typical subject. Note the continuous aperture reduction in No PERT trials (magenta) and a sudden widening of grasp in PERT trials (green) due to the haptic perturbation of the index finger. c, Aperture profiles for PERT and No PERT trials for the same subject. The x-axis is centered on the moment of the perturbation (time 0). The perturbation (p) resulted in a sudden increase of grasp aperture, a perturbation reversal (r), and resumption of aperture closure. d, PMv and aIPS target sites.

Figure 2.

Group mean aperture traces (±1 SE) for each condition in PMv (top) and aIPS (bottom) blocks and TMS latency (columns). Black lines indicate the TMS onset. The gradient bars indicate the expected duration of TMS effects (Thut et al., 2003). Note that in TMS0, the TMS effect overlaps with the onset of the perturbation; in TMS50, it overlaps with the perturbation reversal; and in TMS100, it overlaps with the postreversal compensatory response. Red and blue lines represent the TMS and No TMS conditions, respectively. Solid and dashed lines represent the PERT and No PERT conditions, respectively. Asterisks (250–600 ms) denote significant differences in aperture between TMS + PERT and No TMS + PERT conditions.

Figure 3.

Mean aperture traces for PERT trials in each subject for the PMv-TMS50 condition. In each subject, TMS led to a significant overestimation of grasp aperture for at least two consecutive time bins (100 ms).

Figure 4.

Group effect for PMv-TMS50 for aperture (top) and rate of aperture closure (bottom) in the PERT condition. A significant increase in aperture closure rate at 200 ms (bottom, first asterisk) led to a modulation in aperture closure that persisted through the 250–600 ms interval (top). Consequently, the rate of aperture closure slowed toward the end of the movement in the TMS condition (bottom, last two asterisks) to prevent overclosing before object contact. All designations are as in Figure 2.